Modeling of Soil Nitrification Responses to Temperature Reveals Thermodynamic Differences Between Ammonia-Oxidizing Activity of Archaea and Bacteria
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The ISME Journal (2017) 11, 896–908 © 2017 International Society for Microbial Ecology All rights reserved 1751-7362/17 www.nature.com/ismej ORIGINAL ARTICLE Modeling of soil nitrification responses to temperature reveals thermodynamic differences between ammonia-oxidizing activity of archaea and bacteria Anne E Taylor1, Andrew T Giguere1, Conor M Zoebelein2, David D Myrold1 and Peter J Bottomley1,3 1Department of Crop and Soil Science, Oregon State University, Corvallis, OR, USA; 2Department of Environmental Engineering, Oregon State University, Corvallis, OR, USA and 3Department of Microbiology, Oregon State University, Corvallis, OR, USA Soil nitrification potential (NP) activities of ammonia-oxidizing archaea and bacteria (AOA and AOB, respectively) were evaluated across a temperature gradient (4–42 °C) imposed upon eight soils from four different sites in Oregon and modeled with both the macromolecular rate theory and the square root growth models to quantify the thermodynamic responses. There were significant differences in response by the dominant AOA and AOB contributing to the NPs. The optimal temperatures (Topt)for AOA- and AOB-supported NPs were significantly different (Po0.001), with AOA having Topt412 °C greater than AOB. The change in heat capacity associated with the temperature dependence of z z D T D nitrification ( CP) was correlated with opt across the eight soils, and the CP of AOB activity was significantly more negative than that of AOA activity (Po0.01). Model results predicted, and confirmatory experiments showed, a significantly lower minimum temperature (Tmin) and different, albeit very similar, maximum temperature (Tmax) values for AOB than for AOA activity. The results also suggested that there may be different forms of AOA AMO that are active over different temperature ranges with different Tmin, but no evidence of multiple Tmin values within the AOB. Fundamental differences in temperature-influenced properties of nitrification driven by AOA and AOB provides support for the idea that the biochemical processes associated with NH3 oxidation in AOA and AOB differ thermodynamically from each other, and that also might account for the difficulties encountered in attempting to model the response of nitrification to temperature change in soil environments. The ISME Journal (2017) 11, 896–908; doi:10.1038/ismej.2016.179; published online 20 December 2016 Introduction nitrification (Hu et al., 2015, Liu et al., 2015, Sun et al., 2015). For example, growth of pure cultures of Both ammonia-oxidizing archaea (AOA) and bacteria AOB isolates is usually optimal ⩽ 30 °C (Jiang and (AOB) co-habit diverse soils. In some situations, Bakken, 1999), and one AOB, Nitrosomonas cryoto- AOA outnumber AOB by two to three orders of lerans, can grow at 4–5 °C (Jones et al., 1988). These magnitude, and in other cases, their abundances are observations corroborate several studies that showed more similar (Leininger et al., 2006, Adair and the temperature optimum of soil nitrification is often Schwartz, 2008, Schauss et al., 2009, Taylor et al., ⩽ 30 °C (Malhi and McGill, 1982; Dalias et al., 2002; 2012). Considerable debate has occurred about the Avrahami et al., 2003; Fierer et al., 2003), and soil relative contributions of AOA and AOB to soil nitrification has been measured at temperatures as nitrification, and the factors that may influence those low as 2 °C (Cookson et al., 2002). contributions (Schleper, 2010, Hatzenpichler, 2012, However, a few reports have described nitrifica- Prosser and Nicol, 2012). There is direct and indirect tion in soils from western United States and evidence that factors such as increased CO2,N Australia with temperature optima of 35–40 °C concentration and form, pH, and temperature differ- (Myers, 1975; Stark and Firestone, 1996). The entially influence AOA and AOB contributions to isolation of the AOA Nitrososphaera gargensis and Nitrosocaldus yellowstonii from geothermal sources with temperature optima of 46 and 65–72 °C, Correspondence: AE Taylor, Departments of Crop and Soil respectively (de la Torre et al., 2008; Hatzenpichler Science, Oregon State University, 3017 Ag Life Science Building, et al., 2008), and the discovery of AOA soil isolates, Corvallis, OR 97331, USA. Nitrosotalea devanaterra Nd1, ‘Candidatus Nitroso- E-mail: [email protected] ’ Received 11 April 2016; revised 25 October 2016; accepted cosmicus franklandus and Nitrososphaera viennen- 4 November 2016; published online 20 December 2016 sis, growing optimally at 35–40 °C (Tourna et al., Modeling soil nitrification temperature response AE Taylor et al 897 2011; Lehtovirta-Morley et al., 2014; Lehtovirta- brought to the laboratory where they were sieved Morley et al., 2016), led us to speculate that AOA o4.75 mm. The soils were stored at 4 °C before might be primarily responsible for soil nitrification experimentation. ⩾ 30 °C. In a field study, we previously observed increases of AOA numbers, and evidence of their activity, in cropped soils under late summer/early Response of soil NPs to temperature fall conditions when soil temperatures reached NPs were determined on soil samples as described 30–35 °C (Taylor et al., 2012), and studies from a previously (Taylor et al., 2010b), except slurries were – UK agricultural soil incubated at temperatures shaken at a range of temperatures (4 42 °C) in + between 10 and 30 °C showed that the thaumarch- deionized water containing 1 mM NH4. Some NP μ aeal composition (determined by analysis of the treatments included octyne (4 M) to distinguish relative abundance of 16S ribosomal RNA) shifted between AOA and AOB activities, using a procedure during incubation at 25 and 30 °C, whereas there was described by Taylor et al. (2013). AOA are octyne no change in the AOB community composition resistant, and AOB are octyne sensitive (total − (Tourna et al., 2008; Offre et al., 2009). In contrast, nitrification nitrification by octyne-resistant AOA). AOA were enriched from Arctic soils incubated at NP controls were comprised of soil suspensions to μ 20 °C, and rates of nitrification were measured in three which acetylene was added (10 M) to evaluate the possibility of acetylene-resistant heterotrophic nitri- Arctic soils incubated at 15 °C, where AOB amoA − numbers were below detection (Alves et al., 2013). fication, and also to assess the significance of NO3 In previous studies, we showed that the relative consumption due to assimilation or denitrification. Each treatment had three replicates. Accumulation contributions of AOB and AOA to nitrifying activity − − varied among four pairs of noncropped and cropped of NO2+NO3 was monitored over a 3-day interval in soils sampled throughout the state of Oregon (Taylor incubations performed at 4, 10 and 16 °C, whereas 1 day was sufficient for incubations at higher et al., 2013, 2015; Giguere et al., 2015). In this study, − − the AOA and AOB contributions to the nitrification temperatures. The accumulation of NO2+NO3 in the NPs was considered to be the rate of nitrification. potential (NP) of the above-mentioned soils were − NO2 accumulated to various fractions of the total evaluated over a temperature range that they − − annually experience (4–42 °C). We hypothesized that NO2+NO3 in actively nitrifying soil slurries over the AOA and AOB would exhibit different characteristic temperature range, and generally increased as tem- perature increased but did not change the overall responses to temperature, and to quantify these − − rate of NO2+NO3 accumulation. The accumulation of differences we used two models: the square root − − growth model (SQRT) that has been used to relate NO2+NO3 in the 1- or 3-day NPs was linear at all soil respiratory and growth processes to temperature temperatures, indicating that there was no change in (Birgander et al., 2013; van Gestel et al., 2013), and the nitrifier abundance or adaptation/recovery of NP activity over the course of the NP assays. There was the macromolecular rate theory model (MMRT) − utilized by Schipper et al. (2014) to model the no significant NO3 consumption or production in temperature response of a variety of microbial plus acetylene controls (data not shown), indicating − − + activities, including nitrification. all NO2+NO3 accumulation was likely due to NH4- dependent nitrification, and that alternate sinks for − − NO2 or NO3 were not significant under NP Materials and methods conditions. Chemicals Modeling of the nitrification response to temperature Vanadium chloride, 1-octyne (C8) and NH4Cl were obtained from Sigma-Aldrich (St Louis, MO, USA). Each replicate of the NP temperature response data Acetylene was obtained from Airgas (Radnor, was modeled using two methods. The first was the PA, USA). SQRT developed by Ratkowsky et al. (1983) to describe bacterial growth response to temperature, but has been used more recently to describe soil respiratory and growth processes to temperature Collection of soils (Birgander et al., 2013; van Gestel et al., 2013). In the spring of 2014, soil samples, representing Here it was used to model the NP response to different soil types from different climate regions of temperature: Oregon, were collected from cropped fields and pffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi noncropped locations at four locations (three repli- bðTÀTmax Þ Bacterial growth ¼ aTðÞðÀ Tmin 1 À e Þ cates of each) at Oregon State University Agricultural Experimental Stations located in Corvallis, Pendle- ð1Þ ton, Madras and Klamath Falls, Oregon (Taylor et al., Four unknown parameters